A key role for matrix metalloproteinases and neutral sphingomyelinase-2 in transplant vasculopathy triggered by Anti-HLA antibody

Circulation

Volumn 124, Issue 24, 2011, Pages 2725-2734

  Galvani, Sylvain ^a,b   Trayssac, Magali ^a,b   Augé, Nathalie ^a   Thiers, Jean Claude ^a,b   Calise, Denis ^a   Krell, Hans Willi ^c   Sallusto, Federico ^d   Kamar, Nassim ^b,d   Rostaing, Lionel ^b,d   Thomsen, Mogens ^a,e   Nègre Salvayre, Anne ^a   Salvayre, Robert ^a,b  

^a Université de Toulouse   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c ROCHE DIAGNOSTICS GMBH   (Germany)

^d CHU RANGUEIL   (France)

^e Faculté de Médecine Centre Hospitalo universitaire   (France)

Author keywords

anti HLA class I mAb; metalloproteinases; proliferation; smooth muscle cells; transplant vasculopathy

Indexed keywords

BATIMASTAT; GELATINASE A; GW 4869; HLA ANTIBODY; MATRIX METALLOPROTEINASE 14; RO 282653; SMALL INTERFERING RNA; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTERY GRAFT; ARTERY INTIMA PROLIFERATION; ARTICLE; CELL CULTURE; CONCENTRATION RESPONSE; DNA SYNTHESIS; EX VIVO STUDY; GENETIC TRANSFECTION; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; IN VIVO STUDY; MESENTERIC ARTERY; MITOGENESIS; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSPLANT VASCULOPATHY; VASCULAR DISEASE;

ANILINE COMPOUNDS; ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; ARTERIES; BENZYLIDENE COMPOUNDS; CELLS, CULTURED; CONSTRICTION, PATHOLOGIC; DISEASE MODELS, ANIMAL; HLA ANTIGENS; HUMANS; HYPERPLASIA; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 2; MICE; MICE, SCID; MODELS, ANIMAL; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; PIPERAZINES; PYRIMIDINES; RNA, SMALL INTERFERING; SPHINGOMYELIN PHOSPHODIESTERASE; VASCULAR DISEASES; VASCULAR GRAFTING;

EID: 83455162556     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.021790     Document Type: Article

References (45)

1. Hunt SA, Haddad F. The changing face of heart transplantation. J Am Coll Cardiol. 2008;52:587-598.
2. Mitchell RN, Libby P. Vascular remodeling in transplant vasculopathy. Circ Res. 2007;100:967-978. (Pubitemid 46598921)
3. Weis M, von Scheidt W. Coronary artery disease in the transplanted heart. Annu Rev Med. 2000;51:81-100. (Pubitemid 30216027)
4. Lechler RI, Sykes M, Thomson AW, Turka LA. Organ transplantation: how much of the promise has been realized? Nat Med. 2005;11: 605-613. (Pubitemid 40868300)
5. Schmauss D, Weis M. Cardiac allograft vasculopathy: recent developments. Circulation. 2008;117:2131-2141. (Pubitemid 351596195)
6. Russell PS, Chase CM, Colvin RB. Alloantibody-and T cell-mediated immunity in the pathogenesis of transplant arteriosclerosis: lack of progression to sclerotic lesions in B cell-deficient mice. Transplantation. 1997;64:1531-1536. (Pubitemid 28047379)
7. Terasaki PI, Cai J. Humoral theory of transplantation: further evidence. Curr Opin Immunol. 2005;17:541-545. (Pubitemid 41207959)
8. Cai J, Terasaki PI. Humoral theory of transplantation: mechanism, prevention, and treatment. Hum Immunol. 2005;66:334-342. (Pubitemid 40615787)
9. Soleimani B, Lechler RI, Hornick PI, George AJ. Role of alloantibodies in the pathogenesis of graft arteriosclerosis in cardiac transplantation. Am J Transplant. 2006;6:1781-1785. (Pubitemid 44024950)
10. Wehner J, Morrell CN, Reynolds T, Rodriguez ER, Baldwin WM III. Antibody and complement in transplant vasculopathy. Circ Res. 2007; 100:191-203. (Pubitemid 46208719)
11. Jin YP, Jindra PT, Gong KW, Lepin EJ, Reed EF. Anti-HLA class I antibodies activate endothelial cells and promote chronic rejection. Transplantation. 2005;79(suppl):S19-S21. (Pubitemid 40293567)
12. Bian H, Reed EF. Alloantibody-mediated class I signal transduction in endothelial cells and smooth muscle cells: enhancement by IFN-gamma and TNF-alpha. J Immunol. 1999;163:1010-1018. (Pubitemid 29328114)
13. Li F, Atz ME, Reed EF. Human leukocyte antigen antibodies in chronic transplant vasculopathy: mechanisms and pathways. Curr Opin Immunol. 2009;21:557-562.
14. Zhang X, Rozengurt E, Reed EF. HLA class I molecules partner with integriN̈4 to stimulate endothelial cell proliferation and migration. Sci Signal. 2010;3:ra85.
15. Currie M, Zaki AM, Nejat S, Hirsch GM, Lee TD. Immunologic targets in the etiology of allograft vasculopathy: endothelium versus media. Transpl Immunol. 2008;19:120-126.
16. Nagai R, Suzuki T, Aizawa K, Miyamoto S, Amaki T, Kawai-Kowase K, Sekiguchi KI, Kurabayashi M. Phenotypic modulation of vascular smooth muscle cells: dissection of transcriptional regulatory mechanisms. Ann N Y Acad Sci. 2001;947:56-66.
17. Galvani S, Auge N, Calise D, Thiers JC, Canivet C, Kamar N, Rostaing L, Abbal M, Sallusto F, Salvayre R, Bohler T, Zou Y, Stastny P, Negre-Salvayre A, Thomsen M. HLA class I antibodies provoke graft arteriosclerosis in human arteries transplanted into SCID/beige mice. Am J Transplant. 2009;9:2607-2614.
18. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008;9:139-150. (Pubitemid 351158911)
19. Auge N, Maupas-Schwalm F, Elbaz M, Thiers JC, Waysbort A, Itohara S, Krell HW, Salvayre R, Negre-Salvayre A. Role for MMP-2 in oxidized LDL-induced activation of the sphingomyelin/ceramide pathway and smooth muscle cell proliferation. Circulation. 2004;110: 571-578. (Pubitemid 39031175)
20. Tellier E, Negre-Salvayre A, Bocquet B, Itohara S, Hannun YA, Salvayre R, Auge N. Role for furin in TNFalpha-induced activation of the matrix metalloproteinase/sphingolipid mitogenic pathway. Mol Cell Biol. 2007; 27:2997-3007. (Pubitemid 46581313)
21. Coatrieux C, Sanson M, Negre-Salvayre A, Parini A, Hannun Y, Itohara S, Salvayre R, Auge N. MAO-A-induced mitogenic signaling is mediated by reactive oxygen species, MMP2, and the sphingolipid pathway. Free Radic Biol Med. 2007;43:80-89. (Pubitemid 46874846)
22. Chang C, Werb Z. The many faces of metalloproteases: cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol. 2001;11: S37-S43.
23. Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res. 2002;90: 251-262. (Pubitemid 34633925)
24. Lutz J, Yao Y, Song E, Antus B, Hamar P, Liu S, Heemann U. Inhibition of matrix metalloproteinases during chronic allograft nephropathy in rats. Transplantation. 2005;79:655-661. (Pubitemid 40463171)
25. Tsukioka K, Suzuki J, Fujimori M, Wada Y, Yamaura K, Ito K, Morishita R, Kaneda Y, Isobe M, Amano J. Expression of matrix metalloproteinases in cardiac allograft vasculopathy and its attenuation by anti MMP2 ribozyme gene transfection. Cardiovasc Res. 2002;56:472-478. (Pubitemid 35351569)
26. Hariya A, Takazawa K, Yamamoto T, Amano A. ONO-4817, a novel matrix metalloproteinase inhibitor, attenuates allograft vasculopathy in a rat cardiac transplant. J Heart Lung Transplant. 2004;23: 1163-1169. (Pubitemid 39346232)
27. Berthier C, Marti HP. Metzincins, including matrix metalloproteinases and meprin, in kidney transplantation. Swiss Med Wkly. 2006;136: 789-794. (Pubitemid 46145030)
28. Auge N, Escargueil-Blanc I, Lajoie-Mazenc I, Suc I, Andrieu-Abadie N, Pieraggi MT, Chatelut M, Thiers JC, Jaffrezou JP, Laurent G, Levade T, Negre-Salvayre A, Salvayre R. Potential role for ceramide in mitogenactivated protein kinase activation and proliferation of vascular smooth muscle cells induced by oxidized low density lipoprotein. J Biol Chem. 1998;273:12893-12900. (Pubitemid 28246848)
29. Netzel-Arnett S, Mallya SK, Nagase H, Birkedal-Hansen H, Van Wart HE. Continuously recording fluorescent assays optimized for five human matrix metalloproteinases. Anal Biochem. 1991;195:86-92.
30. Bosma MJ, Carroll AM. The SCID mouse mutant: definition, characterization, and potential uses. Annu Rev Immunol. 1991;9:323-350.
31. Kaplan J, De Domenico I, Ward DM. Chediak-Higashi syndrome. Curr Opin Hematol. 2008;15:22-29. (Pubitemid 350191025)
32. Shibata S, Asano T, Ogura A, Hashimoto N, Hayakawa J, Uetsuka K, Nakayama H, Doi K. SCID-bg mice as xenograft recipients. Lab Anim. 1997;31:163-168. (Pubitemid 27230531)
33. Jefferies WA, MacPherson GG. Expression of the W6/32 HLA epitope by cells of rat, mouse, human and other species: critical dependence on the interaction of specific MHC heavy chains with human or bovine beta 2-microglobulin. Eur J Immunol. 1987;17:1257-1263. (Pubitemid 17148164)
34. Luberto C, Hassler DF, Signorelli P, Okamoto Y, Sawai H, Boros E, Hazen-Martin DJ, Obeid LM, Hannun YA, Smith GK. Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase. J Biol Chem. 2002;277:41128-41139. (Pubitemid 35215704)
35. Reed EF. Signal transduction via MHC class I molecules in endothelial and smooth muscle cells. Crit Rev Immunol. 2003;23:109-128. (Pubitemid 36875476)
36. Kahn-Perles B, Boyer C, Arnold B, Sanderson AR, Ferrier P, Lemonnier FA. Acquisition of HLA class I W6/32 defined antigenic determinant by heavy chains from different species following association with bovine beta 2-microglobulin. J Immunol. 1987;138:2190-2196. (Pubitemid 17046272)
37. Rodrigo E, Lopez-Hoyos M, Escallada R, Fernandez-Fresnedo G, Ruiz JC, Pinera C, Cotorruelo JG, Zubimendi JA, de Francisco AL, Arias M. Circulating levels of MMP-3 and MMP2 in transplant recipients with chronic transplant nephropathy. Nephrol Dial Transplant. 2000;15: 2041-2045.
38. Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol. 2008;75: 346-359. (Pubitemid 350298459)
39. Fingleton B. MMPs as therapeutic targets: still a viable option? Semin Cell Dev Biol. 2008;19:61-68. (Pubitemid 350235985)
40. Yamani MH, Starling RC, Cook DJ, Tuzcu EM, Abdo A, Paul P, Powell K, Ratliff NB, Yu Y, McCarthy PM, Young JB. Donor spontaneous intracerebral hemorrhage is associated with systemic activation of MMP-2 and MMP-9 and subsequent development of coronary vasculopathy in the heart transplant recipient. Circulation. 2003;108: 1724-1728. (Pubitemid 37243661)
41. Strongin AY. Mislocalization and unconventional functions of cellular MMPs in cancer. Cancer Metastasis Rev. 2006;25:87-98. (Pubitemid 43723985)
42. Alvarez SE, Milstien S, Spiegel S. Autocrine and paracrine roles of sphingosine-1-phosphate. Trends Endocrinol Metab. 2007;18:300-307. (Pubitemid 47531961)
43. Japtok L, Kleuser B. The role of sphingosine-1-phosphate receptor modulators in the prevention of transplant rejection and autoimmune diseases. Curr Opin Investig Drugs. 2009;10:1183-1194.
44. Tellides G, Pober JS. Interferon-axis in graft arteriosclerosis. Circ Res. 2007;100:622-632.
45. Tellides G. The adaptive immune responses in cardiac graft arteriosclerosis: deleterious or beneficial? Circulation. 2006;114:1561-1564. (Pubitemid 44547425)